Autonomic neurocristopathy-associated mutations in PHOX2B dysregulate Sox10 expression

Journal of Clinical Investigation

Volumn 122, Issue 9, 2012, Pages 3145-3158

  Nagashimada, Mayumi ^a,b   Ohta, Hiroshi ^a   Li, Chong ^a   Nakao, Kazuki ^a   Uesaka, Toshihiro ^a   Brunet, Jean François ^c   Amiel, Jeanne ^d   Trochet, Delphine ^d   Wakayama, Teruhiko ^a   Enomoto, Hideki ^a,b  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c ECOLE NORMALE SUPÉRIEURE   (France)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; DOPAMINE BETA MONOOXYGENASE; FIBRONECTIN; HOMEODOMAIN PROTEIN; PAIRED LIKE HOMEOBOX 2B PROTEIN; TRANSCRIPTION FACTOR SOX10; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTONOMIC NEUROCRISTOPATHY; AUTONOMIC NEUROPATHY; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; GAIN OF FUNCTION MUTATION; GENE LOCUS; GENE MUTATION; HIRSCHSPRUNG DISEASE; HUMAN; HUMAN CELL; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSACTIVATION;

ANIMALS; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; ENHANCER ELEMENTS, GENETIC; ENTERIC NERVOUS SYSTEM; GANGLIA, SYMPATHETIC; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENE KNOCK-IN TECHNIQUES; HIRSCHSPRUNG DISEASE; HOMEODOMAIN PROTEINS; HYPOVENTILATION; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; NEURAL CREST; NEURAL STEM CELLS; NEUROBLASTOMA; NEUROGLIA; NEURONS; PEPTIDES; PHENOTYPE; REPETITIVE SEQUENCES, AMINO ACID; SEQUENCE DELETION; SLEEP APNEA, CENTRAL; SOXE TRANSCRIPTION FACTORS; SPHEROIDS, CELLULAR; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84865960448     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI63401     Document Type: Article

References (61)

1. Le Douarin NM. Cell line segregation during peripheral nervous system ontogeny. Science. 1986;231(4745):1515-1522. (Pubitemid 16050719)
2. Le Douarin NM, Kalcheim C. The Neural Crest. Cambridge, United Kingdom: Cambridge University Press; 1999.
3. Bolande RP. The neurocristopathies: A unifying concept of disease arising in neural crest. Hum Pathol. 1974;5:409-429.
4. Bolande RP. Neurocristopathy: its growth and development in 20 years. Pediatr Pathol Lab Med. 1997;17(1):1-25. (Pubitemid 27065461)
5. Etchevers HC, Amiel J, Lyonnet S. Molecular bases of human neurocristopathies. In: Saint-Jeannet JP, ed. Neural Crest Induction and Differentiation. Georgetown, Texas, USA: Landes Bioscience; 2006:213-234.
6. Maris JM, Matthay KK. Molecular biology of neuroblastoma. J Clin Oncol. 1999;17(7):2264-2279. (Pubitemid 29318861)
7. Maris JM. Recent advances in neuroblastoma. N Engl J Med. 2010;362(23):2202-2211.
8. Janoueix-Lerosey I, Schleiermacher G, Delattre O. Molecular pathogenesis of peripheral neuroblastic tumors. Oncogene. 2010;29(11):1566-1579.
9. Amiel J, et al. Hirschsprung disease, associated syndromes and genetics: a review. J Med Genet. 2008;45(1):1-14. (Pubitemid 351158152)
10. Gozal D. Congenital central hypoventilation syndrome: an update. Pediatr Pulmonol. 1998;26(4):273-282. (Pubitemid 28492289)
11. Rohrer T, Trachsel D, Engelcke G, Hammer J. Congenital central hypoventilation syndrome associated with Hirschsprung's disease and neuroblastoma: case of multiple neurocristopathies. Pediatr Pulmonol. 2002;33(1):71-76. (Pubitemid 34031557)
12. Trochet D, et al. PHOX2B genotype allows for prediction of tumor risk in congenital central hypoventilation syndrome. Am J Hum Genet. 2005;76(3):421-426. (Pubitemid 40250522)
13. Amiel J, et al. Polyalanine expansion and frameshift mutations of the paired-like homeobox gene PHOX2B in congenital central hypoventilation syndrome. Nat Genet. 2003;33(4):459-461. (Pubitemid 36390004)
14. Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature. 1999;399(6734):366-370. (Pubitemid 29318135)
15. Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF. Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development. 1997;124(20):4065-4075. (Pubitemid 27483333)
16. Ohta H, Wakayama T. Generation of normal progeny by intracytoplasmic sperm injection following grafting of testicular tissue from cloned mice that died postnatally. Biol Reprod. 2005;73(3):390-395. (Pubitemid 41170193)
17. Dubreuil V, et al. A human mutation in Phox2b causes lack of CO2 chemosensitivity, fatal central apnea, and specific loss of parafacial neurons. Proc Natl Acad Sci U S A. 2008;105(3):1067-1072. (Pubitemid 351282082)
18. Coppola E, Pattyn A, Guthrie SC, Goridis C, Studer M. Reciprocal gene replacements reveal unique functions for Phox2 genes during neural differentiation. EMBO J. 2005;24(24):4392-4403. (Pubitemid 41828913)
19. Yntema CL, Hammond WS. The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. J Comp Neurol. 1954;101(2):515-541.
20. Young HM, Hearn CJ, Ciampoli D, Southwell BR, Brunet JF, Newgreen DF. A single rostrocaudal colonization of the rodent intestine by enteric neuron precursors is revealed by the expression of Phox2b, Ret, and p75 and by explants grown under the kidney capsule or in organ culture. Dev Biol. 1998;202(1):67-84. (Pubitemid 28467248)
21. Young HM, Ciampoli D, Hsuan J, Canty AJ. Expression of Ret-, p75(NTR)-, Phox2a-, Phox2b-, and tyrosine hydroxylase-immunoreactivity by undifferentiated neural crest-derived cells and different classes of enteric neurons in the embryonic mouse gut. Dev Dyn. 1999;216(2):137-152. (Pubitemid 29471177)
22. Young HM, Bergner AJ, Muller T. Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine. J Comp Neurol. 2003;456(1):1-11. (Pubitemid 36043638)
23. Britsch S, et al. The ErbB2 and ErbB3 receptors and their ligand, neuregulin-1, are essential for development of the sympathetic nervous system. Genes Dev. 1998;12(12):1825-1836. (Pubitemid 28304335)
24. Schneider C, Wicht H, Enderich J, Wegner M, Rohrer H. Bone morphogenetic proteins are required in vivo for the generation of sympathetic neurons. Neuron. 1999;24(4):861-870. (Pubitemid 30017665)
25. Ernsberger U, Reissmann E, Mason I, Rohrer H. The expression of dopamine beta-hydroxylase, tyrosine hydroxylase, and Phox2 transcription factors in sympathetic neurons: evidence for common regulation during noradrenergic induction and diverging regulation later in development. Mech Dev. 2000;92(2):169-177. (Pubitemid 30155912)
26. Callahan T, Young HM, Anderson RB, Enomoto H, Anderson CR. Development of satellite glia in mouse sympathetic ganglia: GDNF and GFR alpha 1 are not essential. Glia. 2008;56(13):1428-1437.
27. Lo LC, Johnson JE, Wuenschell CW, Saito T, Anderson DJ. Mammalian achaete-scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes Dev. 1991;5(9):1524-1537. (Pubitemid 21906059)
28. Enomoto H, Crawford PA, Gorodinsky A, Heuckeroth RO, Johnson EM, Milbrandt J Jr. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development. 2001;128(20):3963- 3974. (Pubitemid 33040604)
29. Joseph NM, et al. The loss of Nf1 transiently promotes self-renewal but not tumorigenesis by neural crest stem cells. Cancer Cell. 2008;13(2):129-140. (Pubitemid 351163162)
30. Seo H, et al. A direct role of the homeodomain proteins Phox2a/2b in noradrenaline neurotransmitter identity determination. J Neurochem. 2002;80(5):905-916. (Pubitemid 34809244)
31. Kim J, Lo L, Dormand E, Anderson DJ. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron. 2003;38(1):17-31. (Pubitemid 36423350)
32. Werner T, Hammer A, Wahlbuhl M, Bosl MR, Wegner M. Multiple conserved regulatory elements with overlapping functions determine Sox10 expression in mouse embryogenesis. Nucleic Acids Res. 2007;35(19):6526-6538. (Pubitemid 350111620)
33. Antonellis A, et al. Identification of neural crest and glial enhancers at the mouse Sox10 locus through transgenesis in zebrafish. PLoS Genet. 2008;4(9):e1000174.
34. Trochet D, et al. Molecular consequences of PHOX2B missense, frameshift and alanine expansion mutations leading to autonomic dysfunction. Hum Mol Genet. 2005;14(23):3697-3708. (Pubitemid 41754669)
35. Cargnin F, et al. PHOX2B regulates its own expression by a transcriptional auto-regulatory mechanism. J Biol Chem. 2005;280(45):37439- 37448. (Pubitemid 41642351)
36. Britsch S, et al. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev. 2001;15(1):66-78. (Pubitemid 32060683)
37. Menezes M, Puri P. Long-term outcome of patients with enterocolitis complicating Hirschsprung's disease. Pediatr Surg Int. 2006;22(4):316-318.
38. van Limpt V, et al. The Phox2B homeobox gene is mutated in sporadic neuroblastomas. Oncogene. 2004;23(57):9280-9288.
39. Mosse YP, et al. Germline PHOX2B mutation in hereditary neuroblastoma. Am J Hum Genet. 2004;75(4):727-730. (Pubitemid 39244788)
40. Trochet D, et al. Germline mutations of the pairedlike homeobox 2B (PHOX2B) gene in neuroblastoma. Am J Hum Genet. 2004;74(4):761-764. (Pubitemid 38420106)
41. Perri P, et al. PHOX2B mutations and genetic predisposition to neuroblastoma. Oncogene. 2005;24(18):3050-3053. (Pubitemid 40675536)
42. Reiff T, Tsarovina K, Majdazari A, Schmidt M, del Pino I, Rohrer H. Neuroblastoma phox2b variants stimulate proliferation and dedifferentiation of immature sympathetic neurons. J Neurosci. 2010;30(3):905-915.
43. Morrison SJ, White PM, Zock C, Anderson DJ. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell. 1999;96(5):737-749. (Pubitemid 29122815)
44. Adameyko I, et al. Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell. 2009;139(2):366-379.
45. Dupin E, Real C, Glavieux-Pardanaud C, Vaigot P, Le Douarin NM. Reversal of developmental restrictions in neural crest lineages: transition from Schwann cells to glial-melanocytic precursors in vitro. Proc Natl Acad Sci U S A. 2003;100(9):5229-5233. (Pubitemid 36542687)
46. Le Douarin NM, Dupin E. Multipotentiality of the neural crest. Curr Opin Genet Dev. 2003;13(5):529-536. (Pubitemid 37204931)
47. Joseph NM, He S, Quintana E, Kim YG, Nunez G, Morrison SJ. Enteric glia are multipotent in culture but primarily form glia in the adult rodent gut. J Clin Invest. 2011;121(9):3398-3411.
48. Widera D, et al. Schwann cells can be reprogrammed to multipotency by culture. Stem Cells Dev. 2011;20(12):2053-2064.
49. Laranjeira C, et al. Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J Clin Invest. 2011;121(9):3412- 3424.
50. Bourdeaut F, et al. In neuroblastic tumours, Schwann cells do not harbour the genetic alterations of neuroblasts but may nevertheless share the same clonal origin. Oncogene. 2008;27(21):3066-3071. (Pubitemid 351668012)
51. Gershon TR, Oppenheimer O, Chin SS, Gerald WL. Temporally regulated neural crest transcription factors distinguish neuroectodermal tumors of varying malignancy and differentiation. Neoplasia. 2005;7(6):575-584. (Pubitemid 40967758)
52. Hansford LM, et al. Neuroblastoma cells isolated from bone marrow metastases contain a naturally enriched tumor-initiating cell. Cancer Res. 2007;67(23):11234-11243. (Pubitemid 350248549)
53. Raabe EH, et al. Prevalence and functional consequence of PHOX2B mutations in neuroblastoma. Oncogene. 2008;27(4):469-476.
54. Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet. 2000;24(4):372-376. (Pubitemid 30187435)
55. Enomoto H, et al. GFRalpha1 expression in cells lacking RET is dispensable for organogenesis and nerve regeneration. Neuron. 2004;44(4):623-636. (Pubitemid 39531227)
56. Dauger S, et al. Phox2b controls the development of peripheral chemoreceptors and afferent visceral pathways. Development. 2003;130(26):6635- 6642. (Pubitemid 38088862)
57. Uesaka T, Jain S, Yonemura S, Uchiyama Y, Milbrandt J, Enomoto H. Conditional ablation of GFRalpha1 in postmigratory enteric neurons triggers unconventional neuronal death in the colon and causes a Hirschsprung's disease phenotype. Development. 2007;134(11):2171-2181. (Pubitemid 46979803)
58. Bixby S, Kruger GM, Mosher JT, Joseph NM, Morrison SJ. Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity. Neuron. 2002;35(4):643-656. (Pubitemid 35223025)
59. Niwa H, Yamamura K, Miyazaki J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene. 1991;108(2):193-199.
60. Sasaki H, Nishizaki Y, Hui C, Nakafuku M, Kondoh H. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development. 1999;126(17):3915-3924. (Pubitemid 29440488)
61. Enomoto H, et al. GFR a1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron. 1998;21(2):317-324. (Pubitemid 28399692)